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Diversification and evolutionary history of brush-tailed mice, Calomyscidae (Rodentia), in southwestern Asia

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Abstract

Brush-tailed mice, family Calomyscidae, are endemic to southwestern Asia and are represented by eight described species and three additional lineages. Although this family includes only a single genus, Calomyscus, in which several molecular phylogenies were recovered as a monophyletic clade, no updated evolutionary survey has been undertaken until now. We present a time-calibrated molecular phylogenetic tree of members of this genus using mitochondrial and nuclear markers. According to our results, divergence of calomyscid species occurred between 5.85 and 3.35 Mya during the Late Miocene and Pliocene. It seems that the species that occur in the eastern part of the range of the family diverged earlier (highest posterior density (HPD) 3.95–7.28 Mya) from congeners than those from the western part (HPD 2.18–4.24 Mya). Furthermore, we provide new insights on a poorly known species, C. grandis, endemic to the Elburz Mountains, including its phylogeny, morphology (geometric morphometric, karyology, and traditional morphometric methods), and distribution. Our findings show greater haplotype diversity than previously reported and extend the known range of C. grandis in northern Iran. Molecular data detects the existence of an additional distinct lineage from the Zagros Mountains, which appears to be differentiated from other lineages of Calomyscus at levels observed between species. Morphologically, compared to other species, the new lineage is the largest brush-tailed mouse and shows a number of remarkable differences in cranial features (e.g., widest cranium and highest mandible) with chromosomal component 2n = 44 and FNa = 62. Higher species diversity of calomyscids around the Iranian Plateau may be the result of geological events and the subsequent aridification during the Pliocene. The Lut Desert and the Zagros Mountains provided barriers and refugal habitat, respectively, that likely contributed to speciation events within the genus. Additional sampling may discover more distinct lineages in the Zagros Mountains or Anatolia and the eastern Mediterranean region.

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Acknowledgments

We would like to thank Reza Sadeghi who have assisted during fieldworks. Also thanks to Hessam Zali for providing some samples. Anonymous reviewers are acknowledged, whose comments contributed to the improvement of the manuscript.

Funding

This work was supported by Project No. 3.39878 in Ferdowsi University of Mashhad in Iran.

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Authors and Affiliations

  1. Department of Biology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

    Elham Rezazadeh, Mansour Aliabadian & Jamshid Darvish

  2. Research Department of Zoological Innovations, Institute of Applied Zoology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

    Mansour Aliabadian

  3. Research Department of Rodentology, Institute of Applied Zoology, Faculty of Science, Ferdowsi University of Mashhad, Mashhad, Iran

    Jamshid Darvish

  4. Department of Biodiversity and Ecosystem Management, Environmental Sciences Research Institute, Shahid Beheshti University, G.C., Evin, Tehran, Iran

    Faraham Ahmadzadeh

Authors
  1. Elham Rezazadeh
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  2. Mansour Aliabadian
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  4. Faraham Ahmadzadeh
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Corresponding author

Correspondence to Mansour Aliabadian.

Ethics declarations

Sampling was performed after approval by the Department of Environment of Iran (agreement number: 93/340). All experiments were carried out according to the directive 2010/63/EEC on the Protection of Animals Used for Experimental and Other Scientific Purposes (protocol available on http://www.ceropath.org/references/rodent_protocols_book).

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Online Resource 1

Bayesian tree resulted from data set of CO1 gene. Posterior probability values from the Bayesian analysis are indicated by asterisk at the > 99% (**) and > 95% (*) significance levels. Numbers on branch indicate posterior probability values (PNG 2207 kb)

High Resolution Image (TIFF 1291 kb)

Online Resource 2

Bayesian tree resulting from data set of combined two mitochondrial Cyt b and CO1 genes. Posterior probability values from the Bayesian analysis are indicated by asterisk at the > 99% (**) significance level. Numbers on branch indicate posterior probability (values greater than 50% was shown) (PNG 224 kb)

High Resolution Image (TIF 548 kb)

Online Resource 3

Bayesian tree resulting from data set of combined two mitochondrial, Cyt b and CO1, and one nuclear, Rbp3, genes. Posterior probability values from the Bayesian analysis are indicated by asterisk at the > 99% (**) significance level. Numbers on branch indicate posterior probability (values greater than 50% was shown) (PNG 262 kb)

High Resolution Image (TIF 476 kb)

Online Resource 4

Median-joining haplotype network of nuclear Rbp3 gene of the genus Calomyscus. Circle sizes are proportional to the number of the same haplotypes observed in the data set; Black circles represent extinct or unsampled haplotypes. Numbers between haplotypes represent mutational steps between haplotypes (PNG 1426 kb)

High Resolution Image (TIFF 693 kb)

Online Resource 5

Skull centroid size variability among ten groups for ventral view of skull. Symbols and whiskers show means and standard deviations; 1- C. grandis; 2- Calomyscus sp. Group G; 3- C. elburzensis; 4- C. bailwardi; 5- Calomyscus sp. Group C; 6- C. hotsoni; 7- C. urartensis;8- Calomyscus sp. Group D; 9- C. cf. bailwardi Group B; 10- C. mystax (PNG 141 kb)

High Resolution Image (TIF 694 kb)

Online Resource 6

Mahalanobis distances between pairs of groups. *: indicated the significant separation between groups (p < 0.0001) (DOCX 14 kb)

Online Resource 7

Summary of Tukey test (ANOVA) of morphometric comparison of C. grandis (1) and Calamyscus sp. Group G (2) with other groups. Values in bold are statistically significant (P < 0.05) (DOCX 22 kb)

Online Resource 8

Median-joining haplotype network of Cyt b gene of C. grandis and Calomyscus sp. Group G. Circle size is relative to haplotype frequency; Black circles represent extinct or unsampled haplotypes. Numbers indicates the number of mutations between haplotypes (PNG 928 kb)

High Resolution Image (TIFF 473 kb)

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Rezazadeh, E., Aliabadian, M., Darvish, J. et al. Diversification and evolutionary history of brush-tailed mice, Calomyscidae (Rodentia), in southwestern Asia. Org Divers Evol 20, 155–170 (2020). https://doi.org/10.1007/s13127-019-00426-y

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